Neuroprotective effects of inhibiting N-methyl-D-aspartate receptors, P2X receptors and the mitogen-activated protein kinase cascade: A quantitative analysis in organotypical hippocampal slice cultures subjected to oxygen and glucose deprivation

Neuroscience

Volumn 136, Issue 3, 2005, Pages 795-810

  Runden Pran E ^a   Tanso R ^b   Haug, F M ^a   Ottersen, O P ^a   Ring, A ^b  

^a UNIVERSITY OF OSLO   (Norway)

^b NORWEGIAN DEFENCE RESEARCH ESTABLISHMENT FFI   (Norway)

Author keywords

Ischemia; MK 801; PD98059; Propidium iodide; Stroke; Suramin

Indexed keywords

1,4 DIAMINO 1,4 BIS(2 AMINOPHENYLTHIO) 2,3 DICYANOBUTADIENE; 2 (2 AMINO 3 METHOXYPHENYL)CHROMONE; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PURINE P2X RECEPTOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL DAMAGE; CELL DEATH; CONTROLLED STUDY; DENTATE GYRUS; GLUCOSE TRANSPORT; HIPPOCAMPUS; MALE; NEUROPROTECTION; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; RAT; SYNAPTIC TRANSMISSION;

ANIMALS; ANIMALS, NEWBORN; ANOXIA; BLOTTING, WESTERN; CELL DEATH; DIZOCILPINE MALEATE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG INTERACTIONS; ENZYME ACTIVATION; ENZYME INHIBITORS; EXCITATORY AMINO ACID ANTAGONISTS; GLUCOSE; HIPPOCAMPUS; MALE; MICROSCOPY, IMMUNOELECTRON; MITOGEN-ACTIVATED PROTEIN KINASES; NEURONS; NEUROPROTECTIVE AGENTS; ORGAN CULTURE TECHNIQUES; PYRIDOXAL PHOSPHATE; RATS; RATS, WISTAR; RECEPTORS, N-METHYL-D-ASPARTATE; RECEPTORS, PURINERGIC P2; TIME FACTORS;

EID: 28844455527     PISSN: 03064522     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2005.08.069     Document Type: Article

References (85)

1. Y. Adamchik, M.V. Frantseva, M. Weisspapir, P.L. Carlen, J.L. Perez Velazquez Methods to induce primary and secondary traumatic damage in organotypic hippocampal slice cultures Brain Res Brain Res Protoc 5 2000 153 158
2. 2+, and calmodulin Cell Signal 14 2002 649 654
3. A. Alessandrini, S. Namura, M.A. Moskowitz, J.V. Bonventre MEK1 protein kinase inhibition protects against damage resulting from focal cerebral ischemia Proc Natl Acad Sci U S A 96 1999 12866 12869
4. D.R. Alessi, A. Cuenda, P. Cohen, D.T. Dudley, A.R. Saltiel PD 098059 is a specific inhibitor of the activation of mitogen-activated protein kinase kinase in vitro and in vivo J Biol Chem 270 1995 27489 27494
5. S. Amadio, N.D. D'Ambrosi, F. Cavaliere, B. Murra, G. Sancesario, G. Bernardi, G. Burnstock, C. Volonté P2 receptor modulation and cytotoxic function in cultured CNS neurons Neuropharmacology 42 2002 489 501
6. M. Arundine, M. Tymianski Molecular mechanisms of calcium-dependent neurodegeneration in excitotoxicity Cell Calcium 34 2003 325 337
7. G.J. Augustine, F. Santamaria, K. Tanaka Local calcium signaling in neurons Neuron 40 2003 331 346
8. H. Benveniste, M.B. Jorgensen, N.H. Diemer, A.J. Hansen Calcium accumulation by glutamate receptor activation is involved in hippocampal cell damage after ischemia Acta Neurol Scand 78 1988 529 536
9. C. Bonde, J. Noraberg, J. Zimmer Nuclear shrinkage and other markers of neuronal cell death after oxygen-glucose deprivation in rat hippocampal slice cultures Neurosci Lett 327 2002 49 52
10. G. Burnstock, G.E. Knight Cellular distribution and functions of P2 receptor subtypes in different systems Int Rev Cytol 240 2004 31 304
11. F. Cavaliere, N. D'Ambrosi, M.T. Ciotti, G. Mancino, G. Sancesario, G. Bernardi, C. Volonte Glucose deprivation and chemical hypoxia neuroprotection by P2 receptor antagonists Neurochem Int 8 2001 189 197
12. 4 receptor and ischemic cell death prevention by P2 antagonists Neuroscience 120 2003 85 98
13. L. Chang, M. Karin Mammalian MAP kinase signalling cascades Nature 410 2001 37 40
14. S.J. Charlton, C.A. Brown, G.A. Weisman, J.T. Turner, L. Erb, M.R. Boarder PPADS and suramin as antagonist at cloned P2Y- and P2U-purinoceptors Br J Pharmacol 118 1996 704 710
15. C.T. Chu, D.J. Levinthal, S.M. Kulich, E.M. Chalovich, D.B. DeFranco Oxidative neuronal injury. The dark side of ERK1/2 Eur J Biochem 271 2004 2060 2066
16. H. Cimarosti, R. Rodnight, A. Tavares, R. Paiva, L. Valentim, E. Rocha, C. Salbego An investigation of the neuroprotective effect of lithium in organotypic slice cultures of rat hippocampus exposed to oxygen and glucose deprivation Neurosci Lett 315 2001 33 36
17. 7 receptor Neuropharmacology 36 1997 1277 1283
18. T. Cronberg, A. Rytter, F. Asztely, A. Soder, T. Wieloch Glucose but not lactate in combination with acidosis aggravates ischemic neuronal death in vitro Stroke 35 2004 753 757
19. R.A. Cunha, A.M. Sebastiao, J.A. Ribeiro Inhibition by ATP of hippocampal synaptic transmission requires localized extracellular catabolism by ecto-nucleotidases into adenosine and channeling to adenosine A1 receptors J Neurosci 18 1998 1987 1995
20. R.A. Cunha, J.A. Ribeiro ATP as a presynaptic modulator Life Sci 68 2000 119 137
21. 2+ stores Neuron 36 2002 787 790
22. T. Eid, M.J. Thomas, D.D. Spencer, E. Runden-Pran, J.C.K. Lai, G.V. Malthankar, J.H. Kim, N.C. Danbolt, O.P. Ottersen, N.C. de Lanerolle Loss of glutamine synthetase in the human epileptogenic hippocampus possible mechanism for raised extracellular glutamate in mesial temporal lobe epilepsy Lancet 363 2004 28 37
23. J.J. Fernandez, M.L. Candenas, M.L. Souto, M.M. Trujillo, M. Norte Okadaic acid, useful tool for studying cellular processes Curr Med Chem 9 2002 229 262
24. B.H. Gähwiler Organotypic cultures of neural tissue Trends Neurosci 11 1988 484 489
25. B.H. Gähwiler, M. Capogna, D. Debanne, R.A. McKinney, S.M. Thompson Organotypic slice cultures a technique has come of age Trends Neurosci 20 1997 471 477
26. M.M. Gehringer Microcystin-LR and okadaic acid-induced cellular effects a dualistic response FEBS Lett 557 2004 1 8
27. V.D. Gerasimov, D.P. Artemenko, O.A. Krishtal Therapeutic time window for the neuroprotective action of MK-801 after decapitation ischemia hippocampal slice data Brain Res 1017 2004 92 97
28. Z. Gerevich, S.J. Borvendeg, W. Schroder, H. Franke, K. Wirkner, W. Norenberg, S. Furst, C. Gillen, P. Illes Inhibition of N-type voltage-activated calcium channels in rat dorsal root ganglion neurons by P2Y receptors is a possible mechanism of ADP-induced analgesia J Neurosci 24 2004 797 807
29. S.S. Grewal, R.D. York, P.J.S. Stork Extracellular-signal-regulated kinase signalling in neurons Curr Opin Neurobiol 9 1999 544 553
30. Z. Gu, Q. Jiang, G. Zhang, Z. Cui, Z. Zhu Diphosphorylation of extracellular signal-regulated kinases and c-Jun N-terminal protein kinases in brain ischemic tolerance in rat Brain Res 860 2000 157 160
31. Z. Gu, Q. Jiang, G. Zhang Extracellular signal-regulated kinase 1/2 activation in hippocampus after cerebral ischemia may not interfere with postischemic cell death Brain Res 901 2001 79 84
32. A.M. Gutierrez, X. Lou, A. Erik, G. Persson, A. Ring Growth hormones reverse desensitization of P2Y(2) receptors in rat mesangial cells Biochem Biophys Res Commun 270 2000 594 599
33. H.L. Haas, O. Selbach Functions of neuronal adenosine receptors Naunyn Schmiedebergs Arch Pharmacol 362 2000 375 381
34. G.E. Hardingham, H. Bading The yin and yang of NMDA receptor signalling Trends Neurosci 26 2003 81 89
35. M. Hetman, A. Gozdz Role of extracellular signal regulated kinases 1 and 2 in neuronal survival Eur J Biochem 271 2004 2050 2055
36. E.S. Hildebrandt-Eriksen, T. Christensen, N.H. Diemer Mild focal cerebral ischemia in the rat. The effect of local temperature on infarct size Neurol Res 24 2002 781 788
37. B.R. Hu, T. Wieloch Tyrosine phosphorylation and activation of mitogen-activated protein kinase in the rat brain following transient cerebral ischemia J Neurochem 62 1994 1357 1367
38. Y. Hu, P.L. Fisette, L.C. Denlinger, A.G. Guadarrama, J.A. Sommer, R.A. Proctor, P.J. Bertics Purinergic receptor modulation of lipopolysaccharide signaling and inducible nitric-oxide synthase expression in RAW 264.7 macrophages J Biol Chem 273 1998 27170 27175
39. P. Illes, J.A. Ribeiro Molecular physiology of P2 receptors in the central nervous system Eur J Pharmacol 483 2004 5 17
40. F. Kato, M. Kawamura, E. Shigetomi, J. Tanaka, K. Inoue ATP- and adenosine-mediated signaling in the central nervous system: synaptic purinoceptors: the stage for ATP to play its "dual-role." J Pharmacol Sci 94 2004 107 111
41. P. Kermer, N. Klocker, M. Bahr Neuronal death after brain injury. Models, mechanisms, and therapeutic strategies in vivo Cell Tissue Res 298 1999 383 395
42. B.S. Khakh, D. Gittermann, D.A. Cockayne, A. Jones ATP modulation of excitatory synapses onto interneurons J Neurosci 23 2003 7426 7437
43. A. Kharlamov, S.C. Jones, D.K. Kim Suramin reduces infarct volume in a model of focal brain ischemia in rats Exp Brain Res 47 2002 353 359
44. E.J. Kidd, C.B. Grahames, J. Simon, A.D. Michel, E.A. Barnard, P.P. Humphrey Localization of P2X purinoceptor transcripts in the rat nervous system Mol Pharmacol 48 1995 569 573
45. T. Kirino Delayed neuronal death Neuropathology 20 2000 S95 S97
46. G. Lambrecht Agonists and antagonists acting at P2X receptors selectivity profiles and functional implications Naunyn Schmiedebergs Arch Pharmacol 362 2000 340 350
47. 7 receptors in ischemic and excitotoxic brain injury in vivo J Cereb Blood Flow Metab 23 2003 381 384
48. F. Lennmyr, S. Karlsson, P. Gerwins, K.A. Ata, A. Terent Activation of mitogen-activated protein kinases in experimental cerebral ischemia Acta Neurol Scand 106 2002 333 340
49. J.H. Laake, F.M. Haug, T. Wieloch, O.P. Ottersen A simple in vitro model of ischemia based on hippocampal slice cultures and propidium iodide fluorescence Brain Res Brain Res Protoc 4 1999 173 184
50. J.H. Laake, Y. Takumi, J. Eidet, I.A. Torgner, B. Roberg, E. Kvamme, O.P. Ottersen Postembedding immunogold labelling reveals subcellular localization and pathway-specific enrichment of phosphate activated glutaminase in rat cerebellum Neuroscience 88 1999 1137 1151
51. P. Mergenthaler, U. Dirnagl, A. Meisel Pathophysiology of stroke lessons from animal models Metab Brain Dis 19 2004 151 167
52. 2+ microdomains in hippocampal neurons J Neurosci 25 2005 558 565
53. B. Murray, A. Alessandrini, A.J. Cole, A.G. Yee, E.J. Furshpan Inhibition of the p44/42 MAP kinase pathway protects hippocampal neurons in a cell-culture model of seizure activity Proc Natl Acad Sci USA 95 1998 11975 11980
54. S. Namura, K. Iihara, S. Takami, I. Nagata, H. Kikuchi, K. Matsushita, M.A. Moskowitz, J.V. Bonventre, A. Alessandrini Intravenous administration of MEK inhibitor U0126 affords brain protection against forebrain ischemia and focal cerebral ischemia Proc Natl Acad Sci USA 98 2001 11569 11574
55. J. Noraberg, B.W. Kristensen, J. Zimmer Markers for neuronal degeneration in organotypic slice cultures Brain Res Brain Res Protoc 3 1999 278 290
56. J. Noraberg Organotypic brain slice cultures an efficient and reliable method for neurotoxicological screening and mechanistic studies Altern Lab Anim 32 2004 329 337
57. W. Nörenberg, P. Illes Neuronal P2X receptors localisation and functional properties Naunyn Schmiedebergs Arch Pharmacol 362 2000 324 339
58. R.A. North, A. Surprenant Pharmacology of cloned P2X receptors Annu Rev Pharmacol Toxicol 40 2000 563 580
59. R.A. North Molecular physiology of P2X receptors Physiol Rev 82 2002 1013 1067
60. L. Papp, T. Balazsa, A. Kofalvi, F. Erdelyi, G. Szabo, E.S. Vizi, B. Sperlagh P2X receptor activation elicits transporter-mediated noradrenaline release from rat hippocampal slices J Pharmacol Exp Ther 310 2004 973 980
61. J.D. Pediani, J.C. McGrath, S.M. Wilson P2Y receptor-mediated Ca2+ signalling in cultures rat aortic smooth muscle cells Br J Pharmacol 126 1999 1660 1666
62. A.K. Pringle, F. Iannotti, G.J. Wilde, J.E. Chad, P.J. Seeley, L.E. Sundstrom Neuroprotection by both NMDA and non-NMDA receptor antagonists in in vitro ischemia Brain Res 755 1997 36 46
63. C. Racca, F.A. Stephenson, P. Streit, J.D. Roberts, P. Somogyi NMDA receptor content of synapses in stratum radiatum of the hippocampal CA1 area J Neurosci 20 2000 2512 2522
64. A.M. Ray, D.E. Owen, M.L. Evans, J.B. Davis, C.D. Benham Caspase inhibitors are functionally neuroprotective against oxygen glucose deprivation induced CA1 death in rat organotypical hippocampal slices Brain Res 867 2000 62 69
65. S.J. Robertson, S.J. Ennion, R.J. Evans, F.A. Edwards Synaptic P2X receptors Curr Opin Neurobiol 11 2001 378 386
66. 4 receptors in the rat hippocampus J Neurosci 25 2005 6286 6295
67. M.E. Rubio, F. Soto Distinct localization of P2X receptors at excitatory postsynaptic specializations J Neurosci 21 2001 641 653
68. E. Rundén, P.O. Seglen, F.M. Haug, O.P. Ottersen, T. Wieloch, M. Shamloo, J.H. Laake Regional selective neuronal degeneration after protein phosphatase inhibition in hippocampal slice cultures evidence for a MAP kinase-dependent mechanism J Neurosci 18 1998 7296 7305
69. E. Rundén-Pran, F.M. Haug, J.F. Storm, O.P. Ottersen BK channel activity determines the extent of cell degeneration after oxygen and glucose deprivation a study in organotypical hippocampal slice cultures Neuroscience 112 2002 277 288
70. J.K. Ryu, J. Kim, S.H. Choi, Y.J. Oh, Y.B. Lee, S.U. Kim, B.K. Jin ATP-induced in vivo neurotoxicity in the rat striatum via P2 receptors Neuroreport 13 2002 1611 1615
71. J.A. Sakoff, A. McCluskey Protein phosphatase inhibition: structure based design: Towards new therapeutic agents Curr Pharm 10 2004 1139 1159
72. B. Schaller, R. Graf Cerebral ischemia and reperfusion the pathophysiologic concept as a basis for clinical therapy J Cereb Blood Flow Metab 24 2004 351 371
73. R. Schmidt-Kastner, T.F. Freund Selective vulnerability of the hippocampus in brain ischemia Neuroscience 40 1991 599 636
74. M. Shamloo, A. Rytter, T. Wieloch Activation of the extracellular signal-regulated protein kinase cascade in the hippocampal CA1 region in a rat model of global cerebral ischemic preconditioning Neuroscience 93 1999 81 88
75. 7 receptor expression in rodent brain J Neurosci 24 2004 6307 6314
76. B. Sperlágh, A. Köfalvi, J. Deuchars, L. Atkinson, C.J. Milligan, N.J. Buckley, E.S. Vizi Involvement of P2X7 receptors in the regulation of neurotransmitter release in the rat hippocampus J Neurochem 81 2002 1196 1211
77. T.W. Stone, J.I. Addae The pharmacological manipulation of glutamate receptors and neuroprotection Eur J Pharmacol 447 2002 285 296
78. L. Stoppini, P.A. Buchs, D. Muller A simple method for organotypic cultures of nervous tissue J Neurosci Methods 37 1991 173 182
79. Y. Takumi, V. Ramirez-Leon, P. Laake, E. Rinvik, O.P. Ottersen Different modes of expression of AMPA and NMDA receptors in hippocampal synapses Nat Neurosci 2 1999 618 624
80. G.E. Torres, T.M. Egan, M.M. Voigt Hetero-oligomeric assembly of P2X receptor subunits. Specificities exist with regard to possible partners J Biol Chem 274 1999 6653 6659
81. C. Volonte, S. Amadio, F. Cavaliere, N. D'Ambrosi, F. Vacca, G. Bernardi Extracellular ATP and neurodegeneration Curr Drug Targets CNS Neurol Disord 2 2003 403 412
82. X. Wang, H. Wang, L. Xu, D.J. Rozanski, T. Sugawara, P.H. Chan, J.M. Trzaskos, G.Z. Feuerstein Significant neuroprotection against ischemic brain injury by inhibition of the MEK1 protein kinase in mice exploration of potential mechanism associated with apoptosis J Pharmacol Exp Ther 304 2003 172 178
83. D. Zemke, J.L. Smith, M.J. Reeves, A. Majid Ischemia and ischemic tolerance in the brain an overview Neurotoxicology 25 2004 895 904
84. Y. Zhu, H.K. Kimelberg Cellular expression of P2Y and beta-AR receptor mRNAs and proteins in freshly isolated astrocytes and tissue sections from the CA1 region of P8-12 rat hippocampus Brain Res Dev Brain Res 148 2004 77 87
85. J. Zimmer, B.W. Kristensen, B. Jakobsen, J. Noraberg Excitatory amino acid neurotoxicity and modulation of glutamate receptor expression in organotypic brain slice cultures Amino Acids 19 2000 7 21